Anaplasma marginale Infection of Dermacentor andersoni Primary Midgut Cell Culture Is Dependent on Fucosylated Glycans

Abstract

Tick midgut is the primary infection site required by tick-borne pathogens to initiate their development for transmission. Despite the biological significance of this organ, cell cultures derived exclusively from tick midgut tissues are unavailable and protocols for generating primary midgut cell cultures have not been described. To study the mechanism of Anaplasma marginale-tick cell interactions, we successfully developed an in vitro Dermacentor andersoni primary midgut cell culture system. Midgut cells were maintained for up to 120 days. We demonstrated the infection of in vitro midgut cells by using an A. marginale omp10::himar1 mutant with continued replication for up to 10 days post-infection. Anaplasma marginale infection of midgut cells regulated the differential expression of tick α-(1,3)-fucosyltransferases A1 and A2. Silencing of α-(1,3)-fucosyltransferase A2 in uninfected midgut cells reduced the display of fucosylated glycans and significantly lowered the susceptibility of midgut cells to A. marginale infection, suggesting that the pathogen utilized core α-(1,3)-fucose of N-glycans to infect tick midgut cells. This is the first report using in vitro primary D. andersoni midgut cells to study A. marginale-tick cell interactions at the molecular level. The primary midgut cell culture system will further facilitate the investigation of tick-pathogen interactions, leading to the development of novel intervention strategies for tick-borne diseases.

De novo assembly and annotation of the Amblyomma hebraeum tick midgut transcriptome response to Ehrlichia ruminantium infection

“…Moreover, α-1,3-fucosyltransferase has been demonstrated to significantly enhance the susceptibility of D . andersoni midgut cells to Anaplasma marginale infection in vitro [ 75 ].…”

“…Previous studies have reported that A. phagocytophilum modulates the expression of α-1,3-fucosyltransferase during the acquisition phase in I. scapularis midgut and gene silencing significantly reduced the pathogen colonization of both tick midgut cells and murine mast cells in vitro [73,74]. Moreover, α-1,3-fucosyltransferase has been demonstrated to significantly enhance the susceptibility of D. andersoni midgut cells to Anaplasma marginale infection in vitro [75].…”

Clinical Value of Glycan Changes in Cerebrospinal Fluid for Evaluation of Post-Neurosurgical Bacterial Meningitis with Hemorrhagic Stroke Patients

“…In previous studies, fucosylation of bacterial related proteins or lipids, which LTL was conjugated, has been widely investigated in the bacterial infections. Vimonish et al [29] found that Anaplasma marginale regulated the differential expression of tick α-(1,3)-fucosyltransferases in midgut cells, indicating that the pathogen utilized core α-(1,3)-fucose of N-glycan to infect tick midgut cells. Sun et al [30] observed a Salmonella neuraminidase-associated compositional shift of macrophage glycocalyx using nano-LCchip QTOF mass cytometry technology.…”